Skip to main content
Top
Published in: Diabetologia 5/2008

Open Access 01-05-2008 | Article

Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study

Authors: L. Prompers, N. Schaper, J. Apelqvist, M. Edmonds, E. Jude, D. Mauricio, L. Uccioli, V. Urbancic, K. Bakker, P. Holstein, A. Jirkovska, A. Piaggesi, G. Ragnarson-Tennvall, H. Reike, M. Spraul, K. Van Acker, J. Van Baal, F. Van Merode, I. Ferreira, M. Huijberts

Published in: Diabetologia | Issue 5/2008

Login to get access

Abstract

Aims/hypothesis

Outcome data on individuals with diabetic foot ulcers are scarce, especially in those with peripheral arterial disease (PAD). We therefore examined the clinical characteristics that best predict poor outcome in a large population of diabetic foot ulcer patients and examined whether such predictors differ between patients with and without PAD.

Methods

Analyses were conducted within the EURODIALE Study, a prospective cohort study of 1,088 diabetic foot ulcer patients across 14 centres in Europe. Multiple logistic regression modelling was used to identify independent predictors of outcome (i.e. non-healing of the foot ulcer).

Results

After 1 year of follow-up, 23% of the patients had not healed. Independent baseline predictors of non-healing in the whole study population were older age, male sex, heart failure, the inability to stand or walk without help, end-stage renal disease, larger ulcer size, peripheral neuropathy and PAD. When analyses were performed according to PAD status, infection emerged as a specific predictor of non-healing in PAD patients only.

Conclusions/interpretation

Predictors of healing differ between patients with and without PAD, suggesting that diabetic foot ulcers with or without concomitant PAD should be defined as two separate disease states. The observed negative impact of infection on healing that was confined to patients with PAD needs further investigation.
Literature
1.
go back to reference Singh N, Armstrong DG, Lipsky BA (2005) Preventing foot ulcers in patients with diabetes. JAMA 293:217–228PubMedCrossRef Singh N, Armstrong DG, Lipsky BA (2005) Preventing foot ulcers in patients with diabetes. JAMA 293:217–228PubMedCrossRef
2.
go back to reference Nabuurs-Franssen MH, Huijberts MS, Nieuwenhuijzen Kruseman AC, Willems J, Schaper NC (2005) Health-related quality of life of diabetic foot ulcer patients and their caregivers. Diabetologia 48:1906–1910PubMedCrossRef Nabuurs-Franssen MH, Huijberts MS, Nieuwenhuijzen Kruseman AC, Willems J, Schaper NC (2005) Health-related quality of life of diabetic foot ulcer patients and their caregivers. Diabetologia 48:1906–1910PubMedCrossRef
3.
go back to reference Apelqvist J, Ragnarson-Tennvall G, Larsson J, Persson U (1995) Long-term costs for foot ulcers in diabetic patients in a multidisciplinary setting. Foot Ankle Int 16:388–394PubMed Apelqvist J, Ragnarson-Tennvall G, Larsson J, Persson U (1995) Long-term costs for foot ulcers in diabetic patients in a multidisciplinary setting. Foot Ankle Int 16:388–394PubMed
4.
go back to reference Apelqvist J, Ragnarson-Tennvall G, Persson U, Larsson J (1994) Diabetic foot ulcers in a multidisciplinary setting. An economic analysis of primary healing and healing with amputation. J Intern Med 235:463–471PubMedCrossRef Apelqvist J, Ragnarson-Tennvall G, Persson U, Larsson J (1994) Diabetic foot ulcers in a multidisciplinary setting. An economic analysis of primary healing and healing with amputation. J Intern Med 235:463–471PubMedCrossRef
5.
go back to reference Ragnarson-Tennvall G, Apelqvist J (2004) Health-economic consequences of diabetic foot lesions. Clin Infect Dis 39(Suppl 2):S132–S139PubMedCrossRef Ragnarson-Tennvall G, Apelqvist J (2004) Health-economic consequences of diabetic foot lesions. Clin Infect Dis 39(Suppl 2):S132–S139PubMedCrossRef
6.
go back to reference Apelqvist J, Bakker K, van Houtum WH, Nabuurs-Franssen MH, Schaper NC (2000) International consensus and practical guidelines on the management and the prevention of the diabetic foot. International Working Group on the Diabetic Foot. Diabetes Metab Res Rev 16(Suppl 1):S84–S92PubMedCrossRef Apelqvist J, Bakker K, van Houtum WH, Nabuurs-Franssen MH, Schaper NC (2000) International consensus and practical guidelines on the management and the prevention of the diabetic foot. International Working Group on the Diabetic Foot. Diabetes Metab Res Rev 16(Suppl 1):S84–S92PubMedCrossRef
7.
go back to reference Prompers L, Huijberts M, Apelqvist J et al (2007) High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale Study. Diabetologia 50:18–25PubMedCrossRef Prompers L, Huijberts M, Apelqvist J et al (2007) High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale Study. Diabetologia 50:18–25PubMedCrossRef
8.
go back to reference Boulton AJ (1996) The pathogenesis of diabetic foot problems: an overview. Diabet Med 13(Suppl 1):S12–S16PubMed Boulton AJ (1996) The pathogenesis of diabetic foot problems: an overview. Diabet Med 13(Suppl 1):S12–S16PubMed
9.
go back to reference Armstrong DG, Lavery LA, Harkless LB (1998) Validation of a diabetic wound classification system. The contribution of depth, infection, and ischemia to risk of amputation. Diabetes Care 21:855–859PubMedCrossRef Armstrong DG, Lavery LA, Harkless LB (1998) Validation of a diabetic wound classification system. The contribution of depth, infection, and ischemia to risk of amputation. Diabetes Care 21:855–859PubMedCrossRef
10.
go back to reference Prompers L, Huijberts M, Apelqvist J et al (2007) Optimal organisation of health care in diabetic foot disease. Introduction to the Eurodiale Study. Int J Low Extrem Wounds 6:11–17PubMedCrossRef Prompers L, Huijberts M, Apelqvist J et al (2007) Optimal organisation of health care in diabetic foot disease. Introduction to the Eurodiale Study. Int J Low Extrem Wounds 6:11–17PubMedCrossRef
11.
go back to reference Schaper NC, Apelqvist J, Bakker K (2003) The international consensus and practical guidelines on the management and prevention of the diabetic foot. Curr Diab Rep 3:475–479PubMedCrossRef Schaper NC, Apelqvist J, Bakker K (2003) The international consensus and practical guidelines on the management and prevention of the diabetic foot. Curr Diab Rep 3:475–479PubMedCrossRef
12.
go back to reference Schaper NC (2004) Diabetic foot ulcer classification system for research purposes: a progress report on criteria for including patients in research studies. Diabetes Metab Res Rev 20(Suppl 1):S90–S95PubMedCrossRef Schaper NC (2004) Diabetic foot ulcer classification system for research purposes: a progress report on criteria for including patients in research studies. Diabetes Metab Res Rev 20(Suppl 1):S90–S95PubMedCrossRef
13.
go back to reference Little R (1992) Regression with missing X’s: a review. J Am Stat Assoc 87:1227–1237CrossRef Little R (1992) Regression with missing X’s: a review. J Am Stat Assoc 87:1227–1237CrossRef
14.
go back to reference Royston P (2005) Multiple imputation of missing values: update of ice. Stata Journal 5:527–536 Royston P (2005) Multiple imputation of missing values: update of ice. Stata Journal 5:527–536
15.
go back to reference van Buuren S, Boshuizen HC, Knook DL (1999) Multiple imputation of missing blood pressure covariates in survival analysis. Stat Med 18:681–694PubMedCrossRef van Buuren S, Boshuizen HC, Knook DL (1999) Multiple imputation of missing blood pressure covariates in survival analysis. Stat Med 18:681–694PubMedCrossRef
16.
go back to reference Rubin D (1987) Multiple imputation for nonresponse in surveys. Wiley, New York Rubin D (1987) Multiple imputation for nonresponse in surveys. Wiley, New York
17.
go back to reference Carlin J, Li N, Greenwood P, Coffey C (2003) Tools for analyzing multiple imputed datasets. Stata Journal 3:226–244 Carlin J, Li N, Greenwood P, Coffey C (2003) Tools for analyzing multiple imputed datasets. Stata Journal 3:226–244
18.
go back to reference Jeffcoate WJ, Chipchase SY, Ince P, Game FL (2006) Assessing the outcome of the management of diabetic foot ulcers using ulcer-related and person-related measures. Diabetes Care 29:1784–1787PubMedCrossRef Jeffcoate WJ, Chipchase SY, Ince P, Game FL (2006) Assessing the outcome of the management of diabetic foot ulcers using ulcer-related and person-related measures. Diabetes Care 29:1784–1787PubMedCrossRef
19.
go back to reference Beckert S, Witte M, Wicke C, Konigsrainer A, Coerper S (2006) A new wound-based severity score for diabetic foot ulcers: a prospective analysis of 1,000 patients. Diabetes Care 29:988–992PubMedCrossRef Beckert S, Witte M, Wicke C, Konigsrainer A, Coerper S (2006) A new wound-based severity score for diabetic foot ulcers: a prospective analysis of 1,000 patients. Diabetes Care 29:988–992PubMedCrossRef
20.
go back to reference Oyibo SO, Jude EB, Tarawneh I et al (2001) The effects of ulcer size and site, patient’s age, sex and type and duration of diabetes on the outcome of diabetic foot ulcers. Diabet Med 18:133–138PubMedCrossRef Oyibo SO, Jude EB, Tarawneh I et al (2001) The effects of ulcer size and site, patient’s age, sex and type and duration of diabetes on the outcome of diabetic foot ulcers. Diabet Med 18:133–138PubMedCrossRef
21.
go back to reference Cardoso CR, Salles GF (2007) Macro and microvascular complications are determinants of increased infection-related mortality in Brazilian type 2 diabetes mellitus patients. Diabetes Res Clin Pract 75:51–58PubMedCrossRef Cardoso CR, Salles GF (2007) Macro and microvascular complications are determinants of increased infection-related mortality in Brazilian type 2 diabetes mellitus patients. Diabetes Res Clin Pract 75:51–58PubMedCrossRef
22.
go back to reference Lipsky BA, Armstrong DG, Citron DM, Tice AD, Morgenstern DE, Abramson MA (2005) Ertapenem versus piperacillin/tazobactam for diabetic foot infections (SIDESTEP): prospective, randomised, controlled, double-blinded, multicentre trial. Lancet 366:1695–1703PubMedCrossRef Lipsky BA, Armstrong DG, Citron DM, Tice AD, Morgenstern DE, Abramson MA (2005) Ertapenem versus piperacillin/tazobactam for diabetic foot infections (SIDESTEP): prospective, randomised, controlled, double-blinded, multicentre trial. Lancet 366:1695–1703PubMedCrossRef
23.
go back to reference Harkless L, Boghossian J, Pollak R et al (2005) An open-label, randomized study comparing efficacy and safety of intravenous piperacillin/tazobactam and ampicillin/sulbactam for infected diabetic foot ulcers. Surg Infect (Larchmt) 6:27–40CrossRef Harkless L, Boghossian J, Pollak R et al (2005) An open-label, randomized study comparing efficacy and safety of intravenous piperacillin/tazobactam and ampicillin/sulbactam for infected diabetic foot ulcers. Surg Infect (Larchmt) 6:27–40CrossRef
24.
go back to reference Raymakers JT, Houben AJ, van der Heyden JJ, Tordoir JH, Kitslaar PJ, Schaper NC (2001) The effect of diabetes and severe ischaemia on the penetration of ceftazidime into tissues of the limb. Diabet Med 18:229–234PubMedCrossRef Raymakers JT, Houben AJ, van der Heyden JJ, Tordoir JH, Kitslaar PJ, Schaper NC (2001) The effect of diabetes and severe ischaemia on the penetration of ceftazidime into tissues of the limb. Diabet Med 18:229–234PubMedCrossRef
25.
go back to reference Morbach S, Quante C, Ochs HR, Gaschler F, Pallast JM, Knevels U (2001) Increased risk of lower-extremity amputation among Caucasian diabetic patients on dialysis. Diabetes Care 24:1689–1690PubMedCrossRef Morbach S, Quante C, Ochs HR, Gaschler F, Pallast JM, Knevels U (2001) Increased risk of lower-extremity amputation among Caucasian diabetic patients on dialysis. Diabetes Care 24:1689–1690PubMedCrossRef
26.
go back to reference Ince P, Kendrick D, Game F, Jeffcoate W (2007) The association between baseline characteristics and the outcome of foot lesions in a UK population with diabetes. Diabet Med 24:977–981PubMedCrossRef Ince P, Kendrick D, Game F, Jeffcoate W (2007) The association between baseline characteristics and the outcome of foot lesions in a UK population with diabetes. Diabet Med 24:977–981PubMedCrossRef
27.
go back to reference Miyajima S, Shirai A, Yamamoto S, Okada N, Matsushita T (2006) Risk factors for major limb amputations in diabetic foot gangrene patients. Diabetes Res Clin Pract 71:272–279PubMedCrossRef Miyajima S, Shirai A, Yamamoto S, Okada N, Matsushita T (2006) Risk factors for major limb amputations in diabetic foot gangrene patients. Diabetes Res Clin Pract 71:272–279PubMedCrossRef
28.
go back to reference Rajagopalan S, Dellegrottaglie S, Furniss AL et al (2006) Peripheral arterial disease in patients with end-stage renal disease: observations from the Dialysis Outcomes and Practice Patterns Study (DOPPS). Circulation 114:1914–1922PubMedCrossRef Rajagopalan S, Dellegrottaglie S, Furniss AL et al (2006) Peripheral arterial disease in patients with end-stage renal disease: observations from the Dialysis Outcomes and Practice Patterns Study (DOPPS). Circulation 114:1914–1922PubMedCrossRef
29.
go back to reference Boufi M, Ghaffari P, Allaire E, Fessi H, Ronco P, Vayssairat M (2006) Foot gangrene in patients with end-stage renal disease: a case control study. Angiology 57:355–361PubMedCrossRef Boufi M, Ghaffari P, Allaire E, Fessi H, Ronco P, Vayssairat M (2006) Foot gangrene in patients with end-stage renal disease: a case control study. Angiology 57:355–361PubMedCrossRef
30.
go back to reference Leskinen Y, Salenius JP, Lehtimaki T, Huhtala H, Saha H (2002) The prevalence of peripheral arterial disease and medial arterial calcification in patients with chronic renal failure: requirements for diagnostics. Am J Kidney Dis 40:472–479PubMedCrossRef Leskinen Y, Salenius JP, Lehtimaki T, Huhtala H, Saha H (2002) The prevalence of peripheral arterial disease and medial arterial calcification in patients with chronic renal failure: requirements for diagnostics. Am J Kidney Dis 40:472–479PubMedCrossRef
31.
go back to reference Gensler SW, Haimovici H, Hoffert P, Steinman C, Beneventano TC (1965) Study of vascular lesions in diabetic, nondiabetic patients. Clinical, arteriographic, and surgical considerations. Arch Surg 91:617–622PubMed Gensler SW, Haimovici H, Hoffert P, Steinman C, Beneventano TC (1965) Study of vascular lesions in diabetic, nondiabetic patients. Clinical, arteriographic, and surgical considerations. Arch Surg 91:617–622PubMed
32.
go back to reference Fejfarova V, Jirkovska A, Petkov V, Boucek P, Skibova J (2004) Comparison of microbial findings and resistance to antibiotics between transplant patients, patients on hemodialysis, and other patients with the diabetic foot. J Diabetes Complications 18:108–112PubMedCrossRef Fejfarova V, Jirkovska A, Petkov V, Boucek P, Skibova J (2004) Comparison of microbial findings and resistance to antibiotics between transplant patients, patients on hemodialysis, and other patients with the diabetic foot. J Diabetes Complications 18:108–112PubMedCrossRef
33.
go back to reference Cheung A, Wong L (2001) Surgical infections in patients with chronic renal failure. Infect Dis Clin North Am 15:775–796PubMedCrossRef Cheung A, Wong L (2001) Surgical infections in patients with chronic renal failure. Infect Dis Clin North Am 15:775–796PubMedCrossRef
34.
go back to reference Richards AM, Floyd DC, Terenghi G, McGrouther DA (1999) Cellular changes in denervated tissue during wound healing in a rat model. Br J Dermatol 140:1093–1099PubMedCrossRef Richards AM, Floyd DC, Terenghi G, McGrouther DA (1999) Cellular changes in denervated tissue during wound healing in a rat model. Br J Dermatol 140:1093–1099PubMedCrossRef
35.
go back to reference Gibran NS, Jang YC, Isik FF et al (2002) Diminished neuropeptide levels contribute to the impaired cutaneous healing response associated with diabetes mellitus. J Surg Res 108:122–128PubMedCrossRef Gibran NS, Jang YC, Isik FF et al (2002) Diminished neuropeptide levels contribute to the impaired cutaneous healing response associated with diabetes mellitus. J Surg Res 108:122–128PubMedCrossRef
36.
go back to reference Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA (2003) Diabetic neuropathic foot ulcers: predicting which ones will not heal. Am J Med 115:627–631PubMedCrossRef Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA (2003) Diabetic neuropathic foot ulcers: predicting which ones will not heal. Am J Med 115:627–631PubMedCrossRef
37.
go back to reference Armstrong DG, Lavery LA, Wu S, Boulton AJ (2005) Evaluation of removable and irremovable cast walkers in the healing of diabetic foot wounds: a randomized controlled trial. Diabetes Care 28:551–554PubMedCrossRef Armstrong DG, Lavery LA, Wu S, Boulton AJ (2005) Evaluation of removable and irremovable cast walkers in the healing of diabetic foot wounds: a randomized controlled trial. Diabetes Care 28:551–554PubMedCrossRef
38.
go back to reference Mueller MJ, Diamond JE, Sinacore DR et al (1989) Total contact casting in treatment of diabetic plantar ulcers. Controlled clinical trial. Diabetes Care 12:384–388PubMedCrossRef Mueller MJ, Diamond JE, Sinacore DR et al (1989) Total contact casting in treatment of diabetic plantar ulcers. Controlled clinical trial. Diabetes Care 12:384–388PubMedCrossRef
39.
go back to reference Nabuurs-Franssen MH, Sleegers R, Huijberts MS et al (2005) Total contact casting of the diabetic foot in daily practice: a prospective follow-up study. Diabetes Care 28:243–247PubMedCrossRef Nabuurs-Franssen MH, Sleegers R, Huijberts MS et al (2005) Total contact casting of the diabetic foot in daily practice: a prospective follow-up study. Diabetes Care 28:243–247PubMedCrossRef
40.
go back to reference Nabuurs-Franssen MH, Huijberts MS, Sleegers R, Schaper NC (2005) Casting of recurrent diabetic foot ulcers: effective and safe? Diabetes Care 28:1493–1494PubMedCrossRef Nabuurs-Franssen MH, Huijberts MS, Sleegers R, Schaper NC (2005) Casting of recurrent diabetic foot ulcers: effective and safe? Diabetes Care 28:1493–1494PubMedCrossRef
Metadata
Title
Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study
Authors
L. Prompers
N. Schaper
J. Apelqvist
M. Edmonds
E. Jude
D. Mauricio
L. Uccioli
V. Urbancic
K. Bakker
P. Holstein
A. Jirkovska
A. Piaggesi
G. Ragnarson-Tennvall
H. Reike
M. Spraul
K. Van Acker
J. Van Baal
F. Van Merode
I. Ferreira
M. Huijberts
Publication date
01-05-2008
Publisher
Springer-Verlag
Published in
Diabetologia / Issue 5/2008
Print ISSN: 0012-186X
Electronic ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-008-0940-0

Other articles of this Issue 5/2008

Diabetologia 5/2008 Go to the issue